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  • 1. Acta Radiologica 44 (2003) 166±171 Copyright # Acta Radiologica 2003Printed in Denmark Á All rights reserved ACTA RADIOLOGICA ISSN 0284-1851RENAL PERFUSION ABNORMALITYCoded harmonic angio US with contrast agentJ. H. KIM1, H. W. EUN2, H. K. LEE3, S. J. PARK3, J. H. SHIN1, J. H. HWANG1, D. E. GOO1 and D. L. CHOI11Department of Radiology, Soonchunhyang University Hospital, Seoul, 2Health Care Center, Samsung Medical Center, SunkyunkwanUniversity, Seoul, 3Department of Radiology, Soonchunhyang University Bucheon Hospital, Bucheon, Kyonggi-Do, Korea. Abstract Purpose: Coded harmonic angio (CHA) US is a recently developed technique Key words: Kidney, neoplasm; that can depict the effects of contrast agents. The purpose of this study was to trauma; infection; CT; harmonic determine the role of this technique in depicting the enhancement patterns of sonography; contrast medium. various renal perfusion abnormalities compared with dynamic CT. Material and Methods: During a 6-month period, various renal lesions Correspondence: Jung Hoon Kim, including renal cell carcinoma (nˆ12), transitional cell carcinoma (nˆ5), acute Department of Radiology, pyelonephritis (nˆ5), and renal trauma (nˆ2) were evaluated with CHA US Soonchunhyang University Hospital, using a microbubble contrast agent. US images were obtained before contrast 657 Hannam-Dong, Youngsan-Ku, administration and with a bolus injection of 4 g of microbubble contrast agent Seoul 140±743, Korea. (300 mg/ml) every 10 s for 1 min and every minute for 5 min. The contrast FAX ‡82 2 795 3928. enhancement patterns of various renal masses were compared with dynamic CT. E-mail: Results: Of 12 renal cell carcinomas, 9 (75%) showed heterogeneous enhance- ment and the remaining 3 (25%) showed homogeneous enhancement. Enhance- Accepted for publication 7 November ment of more than adjacent renal parenchyma was seen 16±252 s after injection. 2002. The duration of enhancement was 13±208 s (mean, 80 s). All transitional cell carcinomas showed peripheral enhancement. Enhancement was seen 22±270 s after injection. The duration of enhancement was 191±238 s (mean, 291 s). Five patients with acute pyelonephritis and 2 with renal trauma showed focal perfu- sion defects not shown on the pre-contrast examinations. Conclusion: CHA US with microbubble contrast agent is an effective US technique for the evaluation of both tumor vascularity and renal perfusion abnormality.In radiographic studies, contrast agents are widely studies describing how the use of microbubbleused to evaluate renal perfusion abnormalities. agents on color and power Doppler US canDynamic enhancement patterns on contrast- improve the detection and characterization of vari-enhanced CT or MR imaging can help in lesion ous renal perfusion abnormalities, including massescharacterization especially in cases of suspected (1, 2, 5, 6, 15, 20±22); however, there are hardly anyrenal masses (11, 13, 23). human studies (9, 10, 16). Since microbubble US contrast agents have The coded harmonic angio (CHA) US techniquebecome available, their efficacy for characterization is a new imaging technology using contrast agentsof focal renal lesions has been the subject of clinical based on digitally encoded US technology. Thisinvestigations (12). There are many experimental imaging mode is particularly useful when imaging166
  • 2. RENAL PERFUSION ABNORMALITY BY CODED HARMONIC ANGIO USthe arterial or venous phases of tumor vascularity or 2±4 MHz curved linear array transducers. Thefor imaging the stimulated acoustic emission signal acoustic power of CHA US was set at the defaultof agents deposited in the tissue (7, 14). setting (maximum mechanical index X, MI). We expected that CHA US with microbubble Before injection of the contrast agent, we deter-contrast agents could effectively depict renal perfu- mined a scanning plane including the renal masssion abnormalities. The purpose of this study was and obtained a CHA US image. If the patient didto determine the role of this technique in various not have an identified renal mass, we determined arenal perfusion abnormalities compared with scanning plane that included the entire kidney. USdynamic CT. images were obtained before contrast administra- tion as well as with a bolus injection of microbubble contrast agent every 10 s for 1 min and every minute Material and Methods for 5 min. All images were taken as static cine loops.During a 6-month period, 24 patients who were We performed interval delay scanning: i.e. we frozereferred for renal US because of clinically or histo- the display between each scanning time and unfrozepathologically diagnosed renal abnormality were it for a very short period (including 2 or 5 frames)examined with CHA US (LogiQ 700 Expert Series; during each scanning time. Throughout the exam-GE Medical Systems) with a microbubble contrast ination, we held the transducer still and unfroze itagent. during the same status of the patients respiration in Twelve patients with renal cell carcinoma, 5 order to maintain the same scanning plane. Thepatients with transitional cell carcinoma, 5 patients time delay from injection and the time at whichwith acute pyelonephritis, and 2 patients with renal the image was obtained were recorded. All imagestrauma were examined. The patients were 21±67 were stored digitally on the hard disk in the US unityears old (mean 45 years). Of the 22 patients, 18 and transferred to a personal computer. The con-were men. All patients gave their full informed trast enhancement patterns of the various renalconsent for the study and institutional review perfusion abnormalities were assessed.board approval was obtained. Two-phase dynamic CT examinations were per- Ten patients with renal cell carcinoma were diag- formed with a CT-W 2000 (Hitachi) unit. Each patientnosed at surgery and 2 were diagnosed at percuta- received 120 ml of nonionic (iopromide, Ultravist 370;neous needle biopsy. All patients with transitional Schering) contrast material intravenously at a rate ofcell carcinoma were diagnosed at surgery. Five 3 ml/s. Early phase and delay phase scans werepatients with acute pyelonephritis were diagnosed obtained 30 and 150 s after the initiation of injectionas follows: 4 by urine culture and 1 by clinical of the contrast material, respectively. All patents had alaboratory data (pyuria and bacteriuria and typical CT examination within 1±3 days of CHA US examin-symptoms including fever, chills, and flank pain) ation. CT examination was performed with a 5-mmalong with typical dynamic CT findings. Two thickness and 1.5 pitch.patients with renal contusion were diagnosed by Analysis: US images were displayed on a compu-means of their clinical history (1 victim of a motor ter screen and were evaluated by two radiologistsvehicle accident and the other victim of violent (H.W.E., S.J.P.) who were blinded to the diagnoses;trauma) along with typical CT findings. decisions were made by consensus. CT images were The microbubble contrast agent (Levovist; evaluated by one reader (D.E.G.) who was blindedSchering), is a suspension of galactose micropar- to the diagnoses and US findings.ticles in sterile water. The microbubbles (2±8 mm in The reviewers determined the diameters and echo-diameter with a mean diameter of 3 mm), which are genicity of the unenhanced US images. Thestabilized in the microparticle suspension, can echogenicity of the tumors was classified as solid,traverse the pulmonary capillary bed. Before the cystic, or mixed (mixed solid and cystic lesion). AllUS examination, this agent was prepared for injec- observations of the enhancement patterns weretion by shaking it for 5±10 s with 11 ml of water. totally subjective and no quantitative substantiationA milky suspension of galactose microparticles and was performed. The contrast enhancement pattern wasmicrobubbles was created by disaggregation of the determined by evaluating the images obtained duringgranules. After allowing it to stand for 2 min for the early enhancement phase, typically 20±60 s afterequilibration, the contrast agent was injected contrast injection. The enhancement patterns of theintravenously as a bolus in a dose of 4 g at a lesions were classified as homogeneous, hetero-concentration of 300 mg/ml flush using a 0.7- or geneous, peripheral, and perfusion defect.0.9-mm peripheral i.v. cannula. The reviewers also determined the patterns of renal CHA US was performed by one examiner mass on dynamic CT, classified as solid, cystic, or(J.H.K.) with a LogiQ 700 apparatus and mixed (mixed solid and cystic lesion). They also 167
  • 3. J. H. KIM ET AL.evaluated the pattern of contrast enhancement of the compared with adjacent renal parenchyma was per-renal mass. The enhancement patterns of the tumors ipheral in 5 patients (100%) (Fig. 2). Enhancementwere classified as homogeneous, heterogeneous, of more than adjacent renal parenchyma was seenperipheral enhancement, and perfusion defect. 22±32 s (mean, 80 s) after injection. The intensity of the tumor diminished progressively from 220 to 270 s (mean, 247 s) after injection. The duration of Results enhancement was 191±238 s (mean, 219 s).The findings in the various renal masses on CHA Two-phase dynamic CT showed mixed pattern inUS and dynamic CT are summarized in Table 1. 3 patients and solid pattern in 2. All patients showed Renal cell carcinoma: The tumor diameters as peripheral enhancement on the delayed phase.measured on US were 17±87 mm (mean, 37 mm). Acute pyelonephritis: US findings in the 5 patientsSix patients had renal cell carcinomas equal to or with acute pyelonephritis included swelling, diffuseless than 30 mm and the remaining 6 tumors were decreased parenchymal echogenicity, and loss oflarger than 30 mm. The echogenicity was solid in 3 corticomedullary differentiation. However, a definitelesions and mixed in 9. focal parenchymal lesion was not detected on US The most common enhancement pattern seen on imaging. After microbubble contrast injection, all 5CHA US with microbubble contrast agent compared patients showed multifocal or segmental parenchy-with adjacent renal parenchyma was heterogeneous mal perfusion defects (Fig. 3). Two-phase dynamicin 9 lesions (75%) (Fig. 1). Homogeneous enhance- CT showed diffuse renal swelling and delayedment was seen in 3 lesions (25%). Enhancement nephrogram in 5 patients, and focal perfusion defectsmore than that of adjacent renal parenchyma was in 4 patients.seen 16±57 s (mean, 30 s) after injection. The intensity Renal trauma: The 2 patients with renal contu-of the tumor diminished progressively from 51 to sion showed swelling and decreased parenchymal252 s (mean, 82 s) after injection. Although the inten- echogenicity on US before contrast administration.sity of enhanced portions of the tumor diminished, After microbubble contrast injection, both patientsthe duration of enhancement was 13±208 s (mean, showed focal parenchymal perfusion defects80 s) (Table 2). (Fig. 4). Two-phase dynamic CT also showed focal Two-phase dynamic CT showed solid pattern in 3 perfusion defects.lesions and mixed pattern in 9. The most commonenhancement pattern was heterogenous in 9 lesions Discussion(75%) and homogeneous in 3 lesions (25%). Theintratumoral enhancement of more than adjacent CHA US is based on digitally encoded US technol-renal parenchyma in the early phase was seen in ogy combining the benefits of B-flow and coded har-11 of 12 patients. monic imaging technology. CHA US uses the receive Transitional cell carcinoma: The tumor diameters decoder, rather than a frequency filter, to suppressas measured on US were 19±80 mm (mean, 40 mm). unwanted fundamental frequency components. TheThe echogenicity was mixed in 3 patients and solid result is a harmonic image with wide band resolu-in 2. The most common enhancement pattern tion, improved sensitivity, and reduced acousticat CHA US with microbubble contrast agent noise. B-flow is a flow imaging technique that Table 1 Comparison of contrast enhancement patterns at CHA US and dynamic CT Enhancement patterns at CHA US Enhancement patterns at CT Patterns Enhancement patterns Patterns Enhancement patternsLesion S M C Ho He PE PD S M C Ho He PE PDRCC, 3 9 3 9 3 9 3 9 nˆ12TCC, 2 3 5 2 3 5 nˆ5APN, 5 4 nˆ5Trauma, 2 2 nˆ2Sˆsolid, MˆMixed, Cˆcystic, Hoˆhomogeneous, Heˆheterogeneous, PEˆperipheral enhancement, PDˆperfusion defect, RCCˆrenal cellcarcinoma, TCCˆtransitional cell carcinoma, APNˆacute pyelonephritis.168
  • 4. RENAL PERFUSION ABNORMALITY BY CODED HARMONIC ANGIO US a b cFig. 1. Renal cell carcinoma with heterogeneous enhancement. a) Delayed CT shows mass with heterogeneous enhancement in the right kidney.b) US before injection of the contrast agent shows a solid and cystic mass (") in the right kidney. c) Contrast-enhanced CHA US image obtained41 s after injection shows intratumoral heterogeneous enhancement. A thick septum is seen with intense enhancement (ˆ A).extends B-mode imaging capabilities to blood flow. aliasing. In addition, their clinical usefulness hasB-flow provides direct visualization of blood echoes not yet been firmly established. Two experimentalwithout imitations of Doppler US (7, 14). studies (6, 22) showed that contrast-enhanced The microbubble contrast agent is a blood pool harmonic US is an effective method for evaluatingagent, so that imaging of the microvascular system renal blood flow changes during acute urinarycan be performed by provoking the collapse of the obstruction and focal perfusion defects in embo-microbubbles with diagnostically used US waves lized kidneys. In another experimental study (5),with high mechanical index (19). In previous reports the use of contrast agent enhanced the depiction(15, 16), only a short-lasting and weak effect could of an area of acute renal visualized after microbubble contrast agent injec- From the results of this study, we believe that thetion. In contrast to liver tissue, no late-phase con- pattern of enhancement on CHA US using a micro-trast effect could be observed in kidney tissue. bubble contrast agent has potentially high sensitiv-Microvascular imaging of the kidney is possible ity and specificity for the diagnosis of various renalonly during the blood pool phase. There are many perfusion abnormalities including masses comparedexperimental studies of the use of microbubble with dynamic CT. In renal cell carcinoma, the mostagents having improved the detection and charac- common enhancement pattern on CHA US withterization of vascularity in various renal lesions microbubble contrast agent was heterogeneous(1, 2, 5, 6, 15, 20±22); however, there are only enhancement. Homogeneous enhancement wasa few applications of microbubble contrast in seen in 3 lesions (25%). While this enhancementhuman kidney described (9, 10, 16). pattern was seen in patients with renal cell carcin- Previous studies (8, 17, 18) have indicated that oma, this pattern did not occur in any nonmalig-both spectral Doppler and color Doppler US can nant lesions. These enhancement patterns areprovide clinically useful information related to similar to dynamic CT.tumor vascularity; however, these imaging modal- In transitional cell carcinoma, peripheral enhance-ities have inherent limitations, such as a lack of ment was observed on interval delay scanning usingsensitivity to slow flow, angle dependency, and CHA US with a microbubble contrast agent. Table 2 Enhancement duration in various renal masses on CHA US with microbubble contrast agent Contrast enhancement time on CHA US with microbubble contrast in SLesion 10 20 30 40 50 60 120 180 240 300RCC, 2 6 7 12 12 7 3 1 0 0 nˆ12TCC, 0 2 3 3 5 5 5 5 2 0 nˆ5Abbreviations as in Table 1. 169
  • 5. J. H. KIM ET AL. a b cFig. 2. Transitional cell carcinoma with peripheral enhancement. a) Delayed CT shows mass with peripheral enhancement in the right kidney.b) US before injection of the contrast agent shows a solid mass in the right kidney ("). c) Contrast-enhanced CHA US image obtained 53 s afterinjection shows a mass with peripheral enhancement (ˆ A). In acute pyelonephritis, focally decreased par- signal on the next transmit firing (3). Each trans-enchymal echogenicity cannot be detected on US. mitted US pulse in interval delay imaging will pro-After microbubble contrast injection, all our duce the best possible harmonic signals because itpatients showed focal or segmental parenchymal can be arranged to allow areas of slow flow to fillperfusion defects. While conventional US has a with intact microbubbles during the imaging pause.very low sensitivity for acute pyelonephritis, CHA The optimal interval delay between each US pulse isUS with microbubble contrast agent is a sensitive not known and may depend on the flow velocity oftechnique. Dynamic CT showed focal or segmental the vasculature of the examined tissue (4). Furtherparenchymal perfusion defects in 4 patients (80%). studies will be necessary to compare various intervalKIM et al. (10) recently performed contrast- delays in imaging for various renal lesions.enhanced pulse inversion harmonic imaging as a There are a few limitations of this study: there is asensitive technique for depicting renal parenchymal small number of cases, dynamic US scanning is onlylesions and abscess formation in patients with acute possible in one scanning plane, there is greater focalpyelonephritis. Both patients with renal contusion zone dependency so that large or multiple massesshowed focal parenchymal perfusion defects after cannot be fully evaluated on CHA US, and intervalcontrast injection, similar to dynamic CT. For accur- delay scanning in the same area is not easy forate differentiation, it is important to look for renal unskilled examiners to perform. On the otherperfusion in the vascular phase (typically 20±60 s hand, CHA US has the advantages of having higherafter bolus contrast injection). Thereafter, one spatial and temporal resolution compared withshould observe enhancement patterns on successive other imaging techniques, and yields simple andscans in order to diagnose various renal perfusion immediate characterization of a newly detectedabnormalities including masses. renal lesion on US examination. When imaging in a high MI mode, it is necessary In conclusion, CHA US with microbubble contrastto wait for the area of interest to be reperfused by agent is an effective US technique for evaluating boththe agent before imaging again to ensure a sufficient tumor vascularity and renal perfusion abnormalities. a b cFig. 3. Acute pyelonephritis with a multifocal perfusion defect. a) Delayed CT shows swelling and multifocal low density in right kidney. b) USbefore injection of the contrast agent shows diffuse swelling (") but no focal lesions in the right kidney. c) Contrast-enhanced CHA US imageobtained 42 s after injection shows multifocal parenchymal perfusion defects (ˆ A).170
  • 6. RENAL PERFUSION ABNORMALITY BY CODED HARMONIC ANGIO USa b cFig. 4. Renal contusion with a focal perfusion defect. a) Delayed CT shows focal perfusion defect in the posterior segment of the left kidney.b) US before injection of the contrast agent shows a swelling and decreased parenchymal echogenicity in the posterior segment of left kidney.c) Contrast-enhanced CHA US image obtained 33 s after injection shows focal parenchymal perfusion defects in posterior segment of the leftkidney (ˆA). ACKNOWLEDGMENT sonographic contrast agent: correlation with computed tomography. J. Ultrasound Med. 2001; 20: 5.We thank Bonnie Hami, University Hospitals of Cleveland, for 11. Lang EK. Comparison of dynamic and conventionalher editorial assistance in the preparation of this manuscript. computed tomography, angiography and ultrasonography in the staging of renal cell carcinoma. Cancer 1984; 54: 2205. REFERENCES 12. Leen E. Ultrasound contrast harmonic imaging of abdom- inal organs. Semin. Ultrasound CT MRI 2001; 22: 11. 1. Abildgaard A, Klùw N-E, Jakobsen JA et al. Effect of 13. London NJM, Messios N, Kinder RB et al. A prospective ultrasound contrast medium in color Doppler and power study of the value of conventional CT, dynamic CT, ultra- Doppler visualization of blood flow in canine kidneys. Acta sonography and arteriography for staging renal carcinoma. Radiol. 1997; 38: 445. Br. J. Urol. 1989; 64: 209. 2. Berger PE, Kuhn JP. CT of blunt abdominal trauma in 14. Otsuki H, Nakatani S, Yamasaki M et al. Intraoperative childhood. AJR 1981; 136: 105. ultrasound arteriography with the coded harmonic angio 3. Burns PN, Wilson SR, Muradali D et al. Intermittent US technique. J. Neurosurg. 2001; 94: 992. harmonic contrast-enhanced imaging and Doppler improve 15. Pugh CR, Arger PH, Sehgal CM. Power, spectral, and color sensitivity and longevity of vessel detection. Radiology flow Doppler enhancement by a new ultrasonographic con- 1996; 201P: 159. trast agent. J. Ultrasound Med. 1996; 15: 843. 4. Burns PN, Wilson SR, Simpson DH et al. Harmonic inter- 16. Puls R, Hosten N, Lemke M. Perfusion abnormalities of val delay imaging: a new ultrasound contrast method for kidney parenchyma: microvascular imaging with contrast- imaging the blood pool volume in the liver. Radiology 1998; enhancement color and power Doppler ultrasonography ± 209P: 189. preliminary results. J. Ultrasound Med. 2000; 19: 817. 5. Cludon M, Barnewolt CE, Taylor GA et al. Renal blood 17. Ramos IM, Taylor KJW, Kier R. et al. Tumor vascular flow in pigs: changes depicted with contrast-enhanced signals in renal masses: detection with Doppler US. Radi- harmonic US imaging during acute urinary obstruction. ology 1988; 168: 633. Radiology 1999; 212: 725. 18. Riccabona M, Szolar D, Preidler K, et al. Renal masses ± 6. Girard MS, Mattrey RF, Baker KG et al. Comparison of evaluation by amplitude coded color Doppler sonography standard and second harmonic B-mode sonography in the and multiphasic contrast-enhanced CT. Acta Radiol. 1999; detection of segmental renal infarction with sonographic 40: 457. contrast in a rabbit model. J. Ultrasound Med. 2000; 19. Robbin ML. Ultrasound contrast agents: a promising 19: 185. future. Radiol. Clin. North Am. 2001; 39: 399. 7. Hong D, Masatoshi K, Hirokazu O et al. Evaluation of 20. Sehgal CM, Arger PH, Pugh CR. Sonographic enhance- posttreatment response of hepatocellular carcinoma with ment of renal cortex by contrast media. J. Ultrasound contrast-enhanced coded phase-inversion harmonic US. Med. 1995; 14: 741. Comparison with dynamic CT. Radiology 2001; 221: 721. 21. Sehgal CM, Arger PH, Pugh CR et al. Comparison of 8. Kier R, Taylor KJW, Feyock AL et al. Renal masses: char- power Doppler and B-scan sonography for renal imaging acterization with Doppler US. Radiology 1990; 176: 703. using a sonographic contrast agent. J. Ultrasound Med. 9. Kim AY, Kim SH, Kim YJ et al. Contrast-enhanced power 1998; 17: 751. Doppler sonography for the differentiation of cystic 22. Taylor GA, Barnewolt CE, Claudon M et al. Depiction of renal lesions: preliminary study. J. Ultrasound Med. 1999; renal perfusion defects with contrast-enhanced harmonic 18: 581. sonography in a porcine model. AJR 1999; 173: 757.10. Kim B, Lim HK, Choi MH et al. Detection of parenchymal 23. Zeman RK, Cronan JJ, Resenfield AT et al. Imaging abnormalities in acute pyelonephritis by pulse inversion approach to the suspected renal mass. Radiol. Clin. North harmonic imaging with or without microbubble ultra- Am. 1985; 23: 503. 171